Whole-exome sequencing unravels genomic signals of climatic adaptation in Douglas-fir

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Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) is attracting attention outside its natural range, including
Europe, due to its ability to cope with climate warming and drought. Throughout its natural range, it grows along
steep gradients of different climates, which is expected to result in spatially varying selection and adaptation to
local climatic conditions. However, signals of climatic adaptation can often be confounded because unraveled
clines covary with signals caused by neutral evolutionary processes such as gene flow and genetic drift.
Consequently, our understanding of how selection and gene flow have shaped phenotypic and genotypic
differentiation in trees is still limited. A 40-year-old Austrian common garden experiment showing a strong association between growth traits and seed source climate, represented by 16 Douglas-fir provenances covering a north-to-south gradient of approx. 1,000 km, was analyzed. Genomic information was obtained by exome capture, resulting in an initial genomic dataset of >90,000 single nucleotide polymorphisms. We used a restrictive and conservative filtering approach that allowed us to include only SNPs and individuals in the environmental association analysis (EAA) that were free of potentially confounding effects (LD, relatedness among trees, heterozygosity deficiency, and deviations from Hardy–Weinberg proportions). We used four conceptually distinct genome scan methods based on FST outlier detection and gene–environment association in order to disentangle truly adaptive SNPs from neutral SNPs. A relatively small proportion of the exome showed a truly adaptive signal (0.01%–0.17%) when population sub-structuring and multiple testing were taken into account. Nevertheless, the unraveled SNP candidates revealed significant relationships with climate at the provenance origins, strongly suggesting that they have featured adaptation in Douglas-fir along a climatic gradient. Two SNPs were found independently by three of the employed algorithms, and one of them is located in close proximity to an annotated gene involved in circadian clock control and photoperiodism, as also found in Populus balsamifera.
Key words: Douglas-fir, climatic adaptation, common garden experiment, exome capture, environmental
association analysis